Pesq. Vet. Bras. 35(6):583-589, junho 2015 DOI: 10.1590/S0100-736X2015000600017
Macroscopic description of the external and middle ear of paca (Cuniculus paca Linnaeus, 1766)1
Leandro L. Martins2*, Ijanete Almeida-Silva3, Maria Rossato3, Adriana A.B. Murashima3, Miguel A. Hyppolito3 and Marcia R.F. Machado4
ABSTRACT.- Martins L.L., Almeida-Silva I., Rossato M., Murashima A.A.B., Hyppolito M.A. & Machado M.R.F. 2015. Macroscopic description of the external and middle ear of paca (Cuniculus paca Linnaeus, 1766). Pesquisa Veterinária Brasileira 35(6):583-589. Depar- tamento de Anatomia Animal, Escola de Veterinária, Universidade de Ingá, Rodovia PR-317 nº 6114, Maringá, PR 87035-510, Brazil. E-mail: [email protected] Paca (Cuniculus paca), one of the largest rodents of the Brazilian fauna, has inherent characteristics of its species which can conribute as a new option for animal experiman- tation. As there is a growing demand for suitable experimental models in audiologic and otologic surgical research, the gross anatomy and ultrastructural ear of this rodent have been analyzed and described in detail. Fifteen adult pacas from the Wild Animals Sector herd of Faculdade de Ciências Agrárias e Veterinárias, Unesp-Jaboticabal, were used in this study. After anesthesia and euthanasia, we evaluated the entire composition of the exter- nal ear, registering and ddescribing the details; the temporal region was often dissected for a better view and detailing of the tympanic bulla which was removed and opened to expose the ear structures analyzed mascroscopically and ultrastructurally. The ear pinna has a triangular and concave shape with irregular ridges and sharp apex. The external au- ditory canal is winding in its path to the tympanic mebrane. The tympanic bulla is is on
and membranous structures bounded by the tympanic membrane and the oval and round the back-bottom of the skull. The middle ear is formed by a cavity region filled with bone ear is similar to the guinea pig and from the viewpoint of experimental model has major advantageswindows. The compared tympanic with membrane the mouse is flatear. and seals the ear canal. The anatomy of the paca INDEX TERMS: Ear, paca, Cuniculus paca, rodent, temporal bone, ultrastructure.
RESUMO.- [Descrição macroscópica da orelha externa e por modelos experimentais apropriados para pesquisas media da paca (Cuniculus paca Linnaeus, 1766).] A paca audiológicas e otológica cirúrgicas foram analisados e des- (Cuniculus paca), um dos maiores roedores da fauna bra- critos em detalhes a anatomia macroscópica e ultraestrutu- sileira, possui características inerentes à sua espécie que ral da orelha desse roedor. Para o estudo, utilizaram-se 15 podem contribuir como uma nova opção de animal expe- animais adultos provenientes do plantel do Setor de Ani- rimental; assim, considerando-se que há crescente busca mais Silvestres da Faculdade de Ciências Agrárias e Vete- rinárias, Unesp-Jaboticabal, Jaboticabal/SP. Após anestesia 1 Received on April 2, 2014. e eutanásia, avaliou-se toda a composição da orelha exter- Accepted for publication on March 8, 2015. na, registrando-se e descrevendo-se os detalhes, também 2 Departamento de Medicina veterinária, Universidade Estadual de Maringá, se dissecou a região temporal para melhor visibilização e Campus de Umuarama, Estrada da Paca s/n, Bairro São Cristóvão, Umuarama, detalhamento da bula timpânica e estas foram removidas e PR 87507-190, Brasil. *Corresponding author: [email protected] - 3 Departamento de Oftalmologia, Otorrinolaringologia e Cirurgia de Cabeça ram analisadas, macroscopicamente e ultraestruturalmen- e Pescoço, Faculdade de Medicina de Ribeirão Preto, Universidade de São te.abertas O pavilhão a fim de auricular expor as apresenta estruturas forma da orelha, triangular as quais e côn fo- Paulo (USP), Av. Bandeirantes 3900, Ribeirão Preto, SP 14049-900, Brazil. 4 Departamento de Morfologia e Fisiologia Animal, Universidade Estadual cava com cristas irregulares e ápice pontiagudo; o conduto Paulista “Julio de Mesquita Filho” (Unesp), Campus de Jaboticabal, Via de auditivo externo é sinuoso em seu trajeto até a membrana Acesso Prof. Paulo Donato Castellane s/n, Jaboticabal, SP 14884-900, Brazil. timpânica; a bula timpânica encontra-se na parte poste-
583 584 Leandro L. Martins et al. rior-inferior do crânio; a orelha média é formada por uma tigate this animal as an experimental model for otologic região cavitária preenchida por estruturas ósseas e mem- research, focusing, on this occasion, on the description of branosas. É delimitada pela membrana timpânica e as jane- the macroscopic anatomy of the external and middle ear las redonda e oval, sendo a membrana timpânica de forma of the paca. plana e que veda todo o conduto auditivo. A anatomia da orelha da paca é semelhante à da cobaia e do ponto de vista MATERIALS AND METHODS de modelo experimental apresenta grandes vantagens em We used ten adult pacas culled for the selection and maintenance comparação com a orelha do rato. of equilibrium between males and females in the breeding stock TERMOS DE INDEXAÇÃO: Orelha, paca, Cuniculus paca, roedor, of the Sector of Wild Animals, Department of Zootechny, Faculty osso temporal, ultraestrutura. of Agrarian and Veterinary Sciences (FCAV), Jaboticabal Campus, Unesp, registered with the Brazilian Institute of the Environment and Renewable Natural Resources (IBAMA) as a breeding site for INTRODUCTION - There is an increasing search for appropriate experimen- tion no. 482508). tal models for the execution of otologic surgeries. Animal specimensThe animals of the were Brazilian euthanized fauna for with scientific an overdose purposes of midazolam (registra models are the most feasible alternative for otology rese- ((1mg/kg body weight) injected intramuscularly, plus a combina- arch, especially in surgeries that require microscopic en- tion of ketamine hydrochloride (20mg/kg body weight) and xyla- largement by involving delicate structures responsible for zine hydrochloride (1.5mg/kg) placed in the same syringe and injected intramuscularly. hearing such as the tympanic membrane and ossicular chain. Different experimental animal models are used such the temporal region of the skull was dissected in order to descri- as chinchillas, guinea pigs, rats, cats, dogs, and monkeys, be theAfter anatomical the verification region of and death, the insertionthe animal of was the decapitatedtympanic bulla. and among others (Browning & Granich 1978, Doyle & Rood The temporal bone was opened with a surgical clamp positioned 1980, Hellstrom et al. 1982, Giebink et al. 1985, Van der on the cervical spine up to the level of the tympanic bulla, which Ven et al. 1999, Piltcher et al. 2002). Each of these animal was located with the aid of the thumbs and then removed from species has advantages and disadvantages according to the the temporal bone. purposes of the study. To expose the cochlea, using the protocol of Albuquerque et Rats and guinea pigs are the animals most frequently al. (2009), we opened the bulla with the aid of a hemostatic clamp used in otologic research. According to Judkins & Li in the region of the posterior aerial sinus (mastoid) following its salience up to the petrous apex. The clamp was then positioned in the use of guinea pigs in this type of study has advantages the external auditory canal and the entire bony part was broken compared to rats. Also, some facility of handling and(1997), of ma- and raised. nipulation and dissection of the guinea pig’s cochlea has The study was approved by the Animal Ethics and Well-Being been observed. The bone fragility of the tympanic bulla of Committee (CEBEA) of FCAV, Jaboticabal Campus, Unesp (proto- the rat favors its opening for the exposure of structures of col no. 004734-09) according to the Ethical Principles of Animal the middle ear and cochlea, but also involves easy destruc- Experimentation adopted by the Brazilian College of Animal Ex- tion when the temporal bone is removed (Albuquerque et perimentation (COBEA). al. 2009). Guinea pigs and chinchillas are characterized as excel- RESULTS lent study models when topical drugs are applied to the In paca the auricle is a mobile cartilaginous structure con- middle ear. However, the cost for the acquisition and main- nected to the skull by skin, muscles and ligaments, with continuity through the external auditory canal up to the a fact that causes the use of this animal to be unviable. In contrast,tenance of guinea a sufficient pigs are number easy to ofmaintain chinchillas with is proper very high, care and hair. Because of its concave shape with irregular cristae as recommended by the guidelines for the care and use of andtympanic a pointed membrane. apex, it presentsIts surface several is covered regions with with fine salient skin laboratory animals of the Institute of Laboratory Animal delimitations (Fig.1A,B). The auricle measures approxi- Resources, Comission on Life Sciences, National Research mately 4.5cm from base to apex. Council, National Academy Press, Washington, DC., 1996 The temporal bone is located in the posteorinferior re- (Wysocki 2005). gion of the skull between the occipital bone caudally, the Swine and dogs are considered to be excellent models parietal bone dorsally and the frontal, palatine, sphenoid, for otology experimentation but they require elaborate fa- maxillary end ethmoid bone rostrally. The tympanic bulla is cilities with high maintenance costs (Damatta 2010). located in the posteroinferior part of the skull (Fig.2). Squa- Representing an alternative as experimental animals, mous bone forms a process that joins a discrete zygomatic the pacas, which are rodents, can become a good option for arch cranially fused with maxillary bone. It can be seen that research purposes. The largest rodent in the Brazilian fau- this bone structure presents a region with an ivory-like as- na (Matamoros 1982), the paca reaches 80 cm in body leng- pect, with rugosities and areas of bone aeration (Fig.3A,B). th and 12 kg in weight (Pachaly et al. 2001). With a mean Located in a rostroventral direction at the base of the survival time of 16 years, this rodent species is present in temporal bone, the tympanic bulla contains the tympanic large part of the Brazilian territory (Lange & Schmidt 2007, - Queirolo et al. 2008). or and large part of the lateral wall of the tympanic cavity, Within this context, we considered it relevant to inves- presentingcavity of the a singlemiddle cavity ear. The or multiple tympanic aerated bulla forms bone spaces.the flo
Pesq. Vet. Bras. 35(6):583-589, junho 2015 Macroscopic description of the external and middle ear of paca (Cuniculus paca Linnaeus, 1766) 585
Fig.1. (A) Schematic drawing of the auricle of an adult paca (num- B) Photograph of the auricle of the paca showing the following structures:bers corresponding (1) Helix, to(2) those Antihelix, of the (3) figure Bridge, on (4) the Concha; side). ((5) Supratragus, (6) Tragus, (7) Intertragic incisures, (8) External auditory canal, (9) Lobule.
Fig.3. (A) The skull of paca, lateral view. (B) emphasis on the: (1) Tympanic bulla, (2) External auditory canal, (3) Squamous bone, (4) Paraoccipital apophysis, (5) Salience of the posterior air sinus, (6) Salience of the anterior air sinus. Fig.2. Skull of the paca, inferior view, with evidence of the location of the right and left tympanic bullae (circle). chlear nerve, running posterolaterally to the latter, and the - dorsal vestibular nerve is located posterolaterally to the the Theear oforifice the paca. of the With external the aid auditory of a speculum canal (EAC), it is possible of a si tonuous visualize aspect, the is tympanic identified membrane in the cartilaginous and the malleus portion posi of- thefacial facial nerve, canal). which In the is locatedposterior between extremity the of orifices the tympanic of the tioned almost vertically in relation to the membrane; the bulladorsal the and subarched superior fossa vestibular is vestigial nerves and (internal the foramen orifice of the of tympanic membrane seals the canal and delimits the end cerebellar artery is located inside it. Its region is delimited of the external ear. The regions located superiorly and late- by the salience of the superior semicircular canal denoted rally to the opening of the EAC present saliences, which are arched eminence. The foramina of the vestibular, cochle- called anterior and posterior air sinuses, respectively. The ar and facial nerves are located anteriorly. In the anterior bone saliences may be described as having the characteris- extremity, the apex of petrous part of temporal bone has a tics of alveolar bone. rounded shape. The foramen of the facial nerve is located on the late- ral surface inferior to the EAC, while the infratympanic fo- the apex of the tympanic bulla in the direction of the apex ramen is found below the EAC (Fig.3B and 4A). The three of petrousThe orifice part of of the temporal canal of bone the auditory (Fig.5B). tube The is middle located ear in - - branous structures. It is delimited by the tympanic mem- oforifices the cochlear of the vestibular, nerve is cochlearthe one andof largest facial nervescircumference are pre braneis formed and by by a thecavitary round region and oval filled windows. with osseous Inside and its mem bony locatedsent in the in themedial inferior portion medial of the portion tympanic in relation bulla. The to theorifice sa- walls it is possible to observe the epitympanic recess which gittal plane and in an anteroinferior position in relation to is located dorsally to the EAC and the tympanic membrane. the coronal plane. The tympanic membrane seals the entire auditory canal The inferior vestibular nerve is located close to the co- in a plane manner and the malleus handle and incus body,
Pesq. Vet. Bras. 35(6):583-589, junho 2015 586 Leandro L. Martins et al.
gosities and regions of bone aeration observed in the paca is not detected in guinea pigs (Wysocki 2005, Albuquerque et al. 2009), rats (Wysocki 2008) or domestic animals. Also, in contrast to guinea pigs (Wysocki 2005, Albuquerque et al. 2009), rats (Wysocki 2008) and domestic animals (Ni-
Fig.4. (A) The tympanic bulla of an adult paca; lateral view sho- wing the following structures: (1) - External auditory canal, (2) External foramen of the facial nerve canal; 16x. (B) The tympa- nic bulla of an adult paca; medial view showing the following structures: (3) Foramen of the cochlear nerve, (4) Foramen of the inferior vestibular nerve, (5) Foramen of the facial nerve, (6) Foramen of the superior vestibular nerve, (7) Subarched fossa, (8) Arched eminence, Arrow = Projection of the auditory tube (apex of petrous part of temporal bone); 16x. articulation), are visualized projecting on the tympanic membrane.fused together The to malleus form the ossicle malleoincudal is attached junction to the tympanic (fibrous membrane by means of its osseous prolongation, denoted malleus handle, and its major bone portion, denoted body, articulates with the incus (Fig.5A). The bone prominences of the anterior and lateral semi- circular canals can be observed in a medial and dorsal po- sition and the horizontal segment of the facial nerve in its bone canal is visualized in a ventral position in relation to these prominences (Fig.5B). The osseous prominence be- tween the oval and round windows, denoted promontory, is observed in the ventral region of the bulla delimiting the middle ear (Fig.5C). The incus, suspended by the suspen- sory ligament, presents a transversally plane body with a concave articular surface with which it joins the body of the malleus. The two extremities of this ossicle are denoted long process and short process of the incus. The long pro- cess of the incus is articulated with the head of the stapes by means of its lenticular surface (capitulum of the stapes). The short process or branch of the incus projects in the di- rection of the canal of the facial nerve (Fig.5B). The stapes, located medially to the incus, consists of an extremity denoted stapedial head (capitulum) and two branches (anterior crus and posterior crus). These bran- ches are fused to the platen of the stapes, a rounded region forming the base of this ossicle, conferring to it, together with the branches, a triangular shape (Fig.6A-C).
DISCUSSION The location of the temporal bone and tympanic bulla in the paca resembles the descriptions of this organ in domes- Fig.5. The middle ear of an adult paca. (A) (1) Tympanic membra- tic animals (Nickel et al. 1979, Nomina Anatomica Veteri- ne, (2) Malleus handle, (3) Malleoincudal junction, (4) Body naria 2005, Dyce et al. 2010, König & Liebich 2011), guinea of the incus, (5) Long branch of the incus, (6) Short branch of the incus, (7) Facial nerve; 16x. (B) (1) Tympanic membrane, pigs (Cooper & Schiller 1975, Oliveira 1982, Wysocki 2005, (2) Malleus handle, (4) Body of the incus, (8) Tendon of the Albuquerque et al. 2009), rats (Wysocki 2008, Albuquer- stapedial muscle, (9) Facial nerve canal; 16x. (C) (2) Malleus, que et al. 2009), and humans ( Didio 1999, Grabowski & (3) Malleoincudal junction, (5) Long branch of the incus, (6) Tortora 2002). Short branch of the incus, (7) Facial nerve, (10) Stapes, (11) The squamous bone with an ivory-like aspect, with ru- Round window, (12) Cochlea (Promontory). 16x.
Pesq. Vet. Bras. 35(6):583-589, junho 2015 Macroscopic description of the external and middle ear of paca (Cuniculus paca Linnaeus, 1766) 587
ckel et al. 1979, Dyce et al. 2010, König & Liebich 2011), the zygomatic arch of the paca is little developed. This fact is probably due to the feeding habits of these animals. It can be seen that the lateral bony portion of the skull of the paca resembles the human temporal bone, preserving characteristics of osseous aeration, with aerated bone of the alveolar type (Grabowski & Tortora, 2002), which are not observed in domestic animals (König & Liebich 2011), rats (Wysocki 2008) or guinea pigs.
bone,Despite as also the reported technical for guinea difficulty pigs in compared the removal to rats of (Al the- buquerquetympanic bulla et al., of 2009),the paca this due rodent to its has fixation advantages to temporal as an experimental model in surgical otologic procedures. These advantages involve the bodily characteristics of pacas re- garding the physique and the similarity of its lateral bony portion to human temporal bone, especially regarding the characteristics of bone aeration (Grabowski & Tortora 2002). The constitution of the external ear of the paca is si- milar to that of most mammalian species (Cooper & Schil- ler 1975, Nomina Anatomica Veterinaria 2005, Dyce et al. 2010, König & Liebich 2011), especially regarding the presence of a concave cartilaginous structure with regions well delimited by its tortuous aspect. The presence of a lo- bule similar to that existing in humans is observed in this structure (Didio 1999, Grabowski & Tortora 2002). The tympanic bulla, in its semispherical format, pre- sents the apex of petrous part of temporal bone (Wysocki 2005), with a rounded shape compared to that of the gui- nea pig (Goksu et al. 1992, Wysocki 2005, Albuquerque et al. 2009) and the rat (Albuquerque et al. 2009). The external auditory canal of the paca resembles that described in most mammalian species (Cooper & Schil- ler 1975, Nomina Anatomica Veterinaria 2005, Dyce et al. 2010, König & Liebich 2011), with the possibility to visua- lize the tympanic membrane and the malleus handle with the aid of an auricular speculum (Nomina Anatomica Vete- rinaria 2005, Dyce et al. 2010, König & Liebich 2011). The diameter of the external auditory canal can be compared to that of the guinea pig, but differs from that of the rat, which is wider. These anatomical characteristics contribute to advantages in surgical interventions in the middle ear (Albuquerque et al. 2009). In the paca, as is also the case for all domestic species (Nomina Anatomica Veterinaria 2005, Dyce et al. 2010, Kö- nig & Liebich 2011), guinea pigs (Cooper & Schiller 1975, Oliveira 1982) and humans (Grabowski & Tortora 2002), the tympanic membrane seals the auditory canal and de- limits the end of the external ear. This aspects represents Fig.6. (A) Photograph of the ossicles of the middle ear of an adult an advantage of the paca over the rat, in which the greater paca showing the following structures. (1) Malleus handle, (2) exposure of the structures of the middle ear favors the fre- Malleoincudal junction, (3) Body of the incus, (4) Long branch quent occurrence of otitis (Albuquerque et al. 2009), im- of the incus, (5) Incudostapedial joint, (6) Posterior crus of pairing the use of this animal in otologic experiments. the stapes, (7) Anterior crus of the stapes, (8) Platen. (B,C) The middle ear ossicles of an adult paca showing the following The tympanic bulla of the paca presents saliences des- structures: (6) Posterior crus of the stapes, (7) Anterior crus cribed as aerial, anterior and posterior sinuses in its supe- of the stapes, (8) Platen, Arrow = Lenticular process; (2) Mal- rior portion and in the portion lateral to the opening of the leoincudal junction, (3) Body of the incus, (4) Long branch of auditory canal, as also observe din the guinea pig (Wysocki the incus; 35x. 2005) and in the rat (Wysocki 2008). However, the charac-
Pesq. Vet. Bras. 35(6):583-589, junho 2015 588 Leandro L. Martins et al. teristics of this region in the paca can be described as being Acknowledgements.- To the Laboratory of Electron Microscopy, Depart- similar to those of alveolar bone, a fact that makes this ani- ment of Cellular and Molecular Biology and Pathogenic Bioagents, to the Laboratory of Experimental Surgery, Department of Surgery and Anatomy, mal an experimental model with the same characteristics Faculty of Medicine of Ribeirão Preto, and to the Laboratory of Anatomy, as those of humans. The medial portion of the tympanic bulla of the paca for technical assistance, and for financial support to FAPESP and CNPq. does not differ from that of the guinea pig (Wysocki 2005) REFERENCES or the rat (Wysocki 2008) regarding the location of the ori- Albuquerque A.A.S., Rossato M., Oliveira J.A.A. & Hyppolito M.A. 2009. 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